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Therapeutic potential of helminths in autoimmune diseases: helminth-derived immune-regulators and immune balance

Abstract

Helminths have accompanied human throughout history by releasing immune-evasion molecules that could counteract an aberrant immune response within the host. In the past decades, helminth infections are becoming less prevalent possibly due to the developed sanitation. Meanwhile, the incidence of autoimmune diseases is increasing, which cannot be exclusively explained by the changes of susceptibility genes. While the hygiene hypothesis casts light on the problem. The infections of helminths are believed to interact with and regulate human immunity with the byproduct of suppressing the autoimmune diseases. Thus, helminths are potential to treat or cure the autoimmune diseases. The therapeutic progresses and possible immune suppression mechanisms are illustrated in the review. The helminths that are studied most intensively include Heligmosomoides polygyrus, Hymenolepis diminuta, Schistosoma mansoni, Trichinella spiralis, and Trichuris suis. Special attentions are paid on the booming animal models and clinical trials that are to detect the efficiency of immune-modulating helminth-derived molecules on autoimmune diseases. These trials provide us with a prosperous clinical perspective, but the precise mechanism of the down-regulatory immune response remains to be clarified. More efforts are needed to be dedicated until these parasite-derived immune modulators could be used in clinic to treat or cure the autoimmune diseases under a standard management.

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References

  1. Ajendra J, Berbudi A, Hoerauf A, Hubner MP (2016) Combination of worm antigen and proinsulin prevents type 1 diabetes in NOD mice after the onset of insulitis. Clin Immunol 164:119–122

  2. Amdare N, Khatri V, Yadav RS, Tarnekar A, Goswami K, Reddy MV (2015) Brugia malayi soluble and excretory-secretory proteins attenuate development of streptozotocin-induced type 1 diabetes in mice. Parasite Immunol 37:624–634

  3. Ashour DS, Othman AA, Shareef MM, Gaballah HH, Mayah WW (2014) Interactions between Trichinella spiralis infection and induced colitis in mice. J Helminthol 88:210–218

  4. Bager P, Vinkel HA, Wohlfahrt J, Melbye M (2012a) Helminth infection does not reduce risk for chronic inflammatory disease in a population-based cohort study. Gastroenterology 142:55–62

  5. Bager P, Vinkel Hansen A, Wohlfahrt J, Melbye M (2012b) Helminth infection does not reduce risk for chronic inflammatory disease in a population-based cohort study. Gastroenterology 142:55–62

  6. Bashi T, Bizzaro G, Ben-Ami Shor D, Blank M, Shoenfeld Y (2015) The mechanisms behind helminth's immunomodulation in autoimmunity. Autoimmun Rev 14:98–104

  7. Becerra-Diaz M, Valderrama-Carvajal H, Terrazas LI (2011) Signal transducers and activators of transcription (STAT) family members in helminth infections. Int J Biol Sci 7:1371–1381

  8. Behnke JM, Eira C, Rogan M, Gilbert FS, Torres J, Miquel J, Lewis JW (2009) Helminth species richness in wild wood mice, Apodemus sylvaticus, is enhanced by the presence of the intestinal nematode Heligmosomoides polygyrus. Parasitology 136:793–804

  9. Berbudi A, Ajendra J, Wardani AP, Hoerauf A, Hubner MP (2016a) Parasitic helminths and their beneficial impact on type 1 and type 2 diabetes. Diabetes Metab Res Rev 32:238–250

  10. Berbudi A et al (2016b) Filarial infection or antigen administration improves glucose tolerance in diet-induced obese mice. J Innate Immun 8:601–616

  11. Berg DJ et al (2002) Rapid development of colitis in NSAID-treated IL-10-deficient mice. Gastroenterology 123:1527–1542

  12. Bhardwaj EK, Else KJ, Rogan MT, Warhurst G (2014) Increased susceptibility to Trichuris muris infection and exacerbation of colitis in Mdr1a−/− mice. World J Gastroenterol 20:1797–1806

  13. Blum AM, Hang L, Setiawan T, Urban JP Jr, Stoyanoff KM, Leung J, Weinstock JV (2012) Heligmosomoides polygyrus bakeri induces tolerogenic dendritic cells that block colitis and prevent antigen-specific gut T cell responses. J Immunol 189:2512–2520

  14. Cabre P, Signate A, Olindo S, Merle H, Caparros-Lefebvre D, Bera O, Smadja D (2005) Role of return migration in the emergence of multiple sclerosis in the French West Indies. Brain 128:2899–2910

  15. Chandy A, Thakur AS, Singh MP, Manigauha A (2011) A review of neglected tropical diseases: filariasis. Asian Pac J Trop Med 4:581–586

  16. Compston A, Coles A (2008) Multiple sclerosis. Lancet 372:1502–1517

  17. Cooke A (2009) Review series on helminths, immune modulation and the hygiene hypothesis: how might infection modulate the onset of type 1 diabetes? Immunology 126:12–17

  18. Cooke A, Tonks P, Jones FM, O'Shea H, Hutchings P, Fulford AJ, Dunne DW (1999) Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol 21:169–176

  19. Correale J, Farez M (2007) Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol 61:97–108

  20. Dabelea D (2009) The accelerating epidemic of childhood diabetes. Lancet 373:1999–2000

  21. Diamanti AP, Manuela Rosado M, Lagana B, D'Amelio R (2016) Microbiota and chronic inflammatory arthritis: an interwoven link. J Transl Med 14:233

  22. Disanto G, Ramagopalan SV (2013) On the sex ratio of multiple sclerosis. Mult Scler 19:3–4

  23. Donskow-Lysoniewska K, Majewski P, Brodaczewska K, Jozwicka K, Doligalska M (2012) Heligmosmoides polygyrus fourth stages induce protection against DSS-induced colitis and change opioid expression in the intestine. Parasite Immunol 34:536–546

  24. Du L et al (2011) The protective effect of the recombinant 53-kDa protein of Trichinella spiralis on experimental colitis in mice. Dig Dis Sci 56:2810–2817

  25. Du L, Wei H, Li L, Shan H, Yu Y, Wang Y, Zhang G (2014) Regulation of recombinant Trichinella spiralis 53-kDa protein (rTsP53) on alternatively activated macrophages via STAT6 but not IL-4Ralpha in vitro. Cell Immunol 288:1–7

  26. El-Wakil HS, Aboushousha TS, El HO, Gamil NB, Mansour T, El-Said H (2002) Effect of Schistosoma mansoni egg deposition on multiple low doses streptozotocin induced insulin dependent diabetes. J Egypt Soc Parasitol 32:987–1002

  27. Espinoza-Jimenez A, Rivera-Montoya I, Cardenas-Arreola R, Moran L, Terrazas LI (2010) Taenia crassiceps infection attenuates multiple low-dose streptozotocin-induced diabetes. J Biomed Biotechnol 2010:850541

  28. Ferreira I et al (2013) Hookworm excretory/secretory products induce interleukin-4 (IL-4)+ IL-10+ CD4+ T cell responses and suppress pathology in a mouse model of colitis. Infect Immun 81:2104–2111

  29. Finlay CM, Stefanska AM, Walsh PT, Mills KHG (2011) Immunoregulatory effects of the excretory-sectretory products of the helminth parasite Fasciola hepatica. Cytokine 56:37–37

  30. Fleming JO, Cook TD (2006) Multiple sclerosis and the hygiene hypothesis. Neurology 67:2085–2086

  31. Fleming JO et al (2011) Probiotic helminth administration in relapsing-remitting multiple sclerosis: a phase 1 study. Mult Scler 17:743–754

  32. Gruden-Movsesijan A, Ilic N, Mostarica-Stojkovic M, Stosic-Grujicic S, Milic M, Sofronic-Milosavljevic L (2008) Trichinella spiralis: modulation of experimental autoimmune encephalomyelitis in DA rats. Exp Parasitol 118:641–647

  33. Hammond KJ, Poulton LD, Palmisano LJ, Silveira PA, Godfrey DI, Baxter AG (1998) alpha/beta-T cell receptor (TCR)+CD4-CD8- (NKT) thymocytes prevent insulin-dependent diabetes mellitus in nonobese diabetic (NOD)/Lt mice by the influence of interleukin (IL)-4 and/or IL-10. J Exp Med 187:1047–1056

  34. Hang L et al (2010) Heligmosomoides polygyrus infection can inhibit colitis through direct interaction with innate immunity. J Immunol 185:3184–3189

  35. Hang L, Blum AM, Setiawan T, Urban JP Jr, Stoyanoff KM, Weinstock JV (2013) Heligmosomoides polygyrus bakeri infection activates colonic Foxp3+ T cells enhancing their capacity to prevent colitis. J Immunol 191:1927–1934

  36. Harnett MM, Melendez AJ, Harnett W (2010) The therapeutic potential of the filarial nematode-derived immunodulator, ES-62 in inflammatory disease. Clin Exp Immunol 159:256–267

  37. Hasby EA, Hasby Saad MA, Shohieb Z, El Noby K (2015) FoxP3+ T regulatory cells and immunomodulation after Schistosoma mansoni egg antigen immunization in experimental model of inflammatory bowel disease. Cell Immunol 295:67–76

  38. Hewitson JP, Grainger JR, Maizels RM (2009) Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 167:1–11

  39. Heylen M, Ruyssers NE, De Man JG, Timmermans JP, Pelckmans PA, Moreels TG, De Winter BY (2014) Worm proteins of Schistosoma mansoni reduce the severity of experimental chronic colitis in mice by suppressing colonic proinflammatory immune responses. PLoS One 9:e110002

  40. Hubner MP, Stocker JT, Mitre E (2009) Inhibition of type 1 diabetes in filaria-infected non-obese diabetic mice is associated with a T helper type 2 shift and induction of FoxP3+ regulatory T cells. Immunology 127:512–522

  41. Hubner MP et al (2012) Helminth protection against autoimmune diabetes in nonobese diabetic mice is independent of a type 2 immune shift and requires TGF-beta. J Immunol 188:559–568

  42. Hunter MM, Wang A, Parhar KS, Johnston MJ, Van Rooijen N, Beck PL, McKay DM (2010) In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 138:1395–1405

  43. Imai S, Tezuka H, Fujita K (2001) A factor of inducing IgE from a filarial parasite prevents insulin-dependent diabetes mellitus in nonobese diabetic mice. Biochem Biophys Res Commun 286:1051–1058

  44. Johnston MJ, Wang A, Catarino ME, Ball L, Phan VC, MacDonald JA, McKay DM (2010) Extracts of the rat tapeworm, Hymenolepis diminuta, suppress macrophage activation in vitro and alleviate chemically induced colitis in mice. Infect Immun 78:1364–1375

  45. Kaser A, Zeissig S, Blumberg RS (2010) Inflammatory bowel disease. Annu Rev Immunol 28:573–621

  46. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483

  47. Kennel De March A, De Bouwerie M, Kolopp-Sarda MN, Faure GC, Bene MC, Bernard CC (2003) Anti-myelin oligodendrocyte glycoprotein B-cell responses in multiple sclerosis. J Neuroimmunol 135:117–125

  48. Khan N, Smith MT (2014) Multiple sclerosis-induced neuropathic pain: pharmacological management and pathophysiological insights from rodent EAE models. Inflammopharmacology 22:1–22

  49. Khan WI, Blennerhasset PA, Varghese AK, Chowdhury SK, Omsted P, Deng Y, Collins SM (2002) Intestinal nematode infection ameliorates experimental colitis in mice. Infect Immun 70:5931–5937

  50. Khatri V, Amdare N, Tarnekar A, Goswami K, Reddy MV (2015) Brugia malayi cystatin therapeutically ameliorates dextran sulfate sodium-induced colitis in mice. J Dig Dis 16:585–594

  51. Kondrashova A, Seiskari T, Ilonen J, Knip M, Hyoty H (2013) The ‘Hygiene hypothesis’ and the sharp gradient in the incidence of autoimmune and allergic diseases between Russian Karelia and Finland. APMIS 121:478–493

  52. Kringel H, Roepstorff A (2006) Trichuris suis population dynamics following a primary experimental infection. Vet Parasitol 139:132–139

  53. Krishna CS, Srikanta S (2015) Type 1 diabetes pathogenesis—prevention??? Indian J Endocrinol Metab 19:S58–S63

  54. Kuhbacher T, Folsch UR (2007) Practical guidelines for the treatment of inflammatory bowel disease. World J Gastroenterol 13:1149–1155

  55. Lalive PH et al (2006) Antibodies to native myelin oligodendrocyte glycoprotein are serologic markers of early inflammation in multiple sclerosis. Proc Natl Acad Sci U S A 103:2280–2285

  56. Leibowitz U, Antonovsky A, Medalie JM, Smith HA, Halpern L, Alter M (1966) Epidemiological study of multiple sclerosis in Israel. II Multiple sclerosis and level of sanitation. J Neurol Neurosurg Psychiatry 29:60–68

  57. Leung J, Hang L, Blum A, Setiawan T, Stoyanoff K, Weinstock J (2012) Heligmosomoides polygyrus abrogates antigen-specific gut injury in a murine model of inflammatory bowel disease. Inflamm Bowel Dis 18:1447–1455

  58. Lin L, Zhang J (2017) Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol 18:2

  59. Liu Q et al (2009) Helminth infection can reduce insulitis and type 1 diabetes through CD25- and IL-10-independent mechanisms. Infect Immun 77:5347–5358

  60. Lund ME, O'Brien BA, Hutchinson AT, Robinson MW, Simpson AM, Dalton JP, Donnelly S (2014) Secreted proteins from the helminth Fasciola hepatica inhibit the initiation of autoreactive T cell responses and prevent diabetes in the NOD mouse. PLoS One 9:e86289

  61. Maloy KJ, Powrie F (2011) Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474:298–306

  62. Matisz CE, Leung G, Reyes JL, Wang A, Sharkey KA, McKay DM (2015) Adoptive transfer of helminth antigen-pulsed dendritic cells protects against the development of experimental colitis in mice. Eur J Immunol 45:3126–3139

  63. Matsuoka K, Hibi T (2013) Treatment guidelines in inflammatory bowel disease: the Japanese perspectives. Dig Dis 31:363–367

  64. Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF (2008) Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest 118:3420–3430

  65. Melon A, Wang A, Phan V, McKay DM (2010) Infection with Hymenolepis diminuta is more effective than daily corticosteroids in blocking chemically induced colitis in mice. J Biomed Biotechnol 2010:384523

  66. Motomura Y, Wang H, Deng Y, El-Sharkawy RT, Verdu EF, Khan WI (2009) Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clin Exp Immunol 155:88–95

  67. Osada Y, Kanazawa T (2010) Parasitic helminths: new weapons against immunological disorders. J Biomed Biotechnol 2010:743758

  68. Ostanin DV et al (2009) T cell transfer model of chronic colitis: concepts, considerations, and tricks of the trade. Am J Physiol Gastrointest Liver Physiol 296:G135–G146

  69. van Panhuis WG et al (2013) Contagious diseases in the United States from 1888 to the present. N Engl J Med 369:2152–2158

  70. Patt H, Bandgar T, Lila A, Shah N (2013) Management issues with exogenous steroid therapy. Indian J Endocrinol Metab 17:S612–S617

  71. Peres RS et al (2013) Previous contact with Strongyloides venezuelensis contributed to prevent insulitis in MLD-STZ diabetes. Exp Parasitol 134:183–189

  72. Ponder A, Long MD (2013) A clinical review of recent findings in the epidemiology of inflammatory bowel disease. Clin Epidemiol 5:237–247

  73. Reyes JL et al (2015) Splenic B cells from Hymenolepis diminuta-infected mice ameliorate colitis independent of T cells and via cooperation with macrophages. J Immunol 194:364–378

  74. Reyes JL et al (2016a) IL-22 restrains tapeworm-mediated protection against experimental colitis via regulation of IL-25 expression. PLoS Pathog 12:e1005481

  75. Reyes JL et al (2016b) Treatment with Cestode parasite antigens results in recruitment of CCR2+ myeloid cells, the adoptive transfer of which ameliorates colitis. Infect Immun 84:3471–3483

  76. Ruyssers NE et al (2010) Schistosoma mansoni proteins attenuate gastrointestinal motility disturbances during experimental colitis in mice. World J Gastroenterol 16:703–712

  77. Saunders KA, Raine T, Cooke A, Lawrence CE (2007) Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun 75:397–407

  78. Scholmerich J et al (2016) A randomised, double-blind, placebo-controlled trial of Trichuris suis ova in active Crohn’s disease. J Crohns Colitis 11:390–399

  79. Seiskari T et al (2007) Allergic sensitization and microbial load--a comparison between Finland and Russian Karelia. Clin Exp Immunol 148:47–52

  80. Sewell D, Qing Z, Reinke E, Elliot D, Weinstock J, Sandor M, Fabry Z (2003) Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol 15:59–69

  81. Simon F, Prieto G, Muro A, Cancrini G, Cordero M, Genchi C (1997) Human humoral immune response to Dirofilaria species. Parassitologia 39:397–400

  82. Sofronic-Milosavljevic LJ, Radovic I, Ilic N, Majstorovic I, Cvetkovic J, Gruden-Movsesijan A (2013) Application of dendritic cells stimulated with Trichinella spiralis excretory-secretory antigens alleviates experimental autoimmune encephalomyelitis. Med Microbiol Immunol 202:239–249

  83. Stefanska AM, Finlay CM, Mielke LA, Walsh KP, Walsh PT, Mills KH (2011) Immunomodulatory molecules from Fasciola hepatica directly suppress activation of IL-17-producing gamma delta and CD4 T cells that mediate autoimmune disease. Immunology 135:201–201

  84. Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299:1259–1260

  85. Summers RW, Elliott DE, Urban JF Jr, Thompson RA, Weinstock JV (2005) Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128:825–832

  86. Szkudlapski D et al (2014) The emerging role of helminths in treatment of the inflammatory bowel disorders. J Physiol Pharmacol 65:741–751

  87. Tanabe M (2003) Haemostatic abnormalities in hepatosplenic schistosomiasis mansoni. Parasitol Int 52:351–359

  88. Terrazas LI, Montero D, Terrazas CA, Reyes JL, Rodriguez-Sosa M (2005) Role of the programmed death-1 pathway in the suppressive activity of alternatively activated macrophages in experimental cysticercosis. Int J Parasitol 35:1349–1358

  89. Tezuka H, Imai S, Muto R, Furuhashi Y, Fujita K (2002) Recombinant Dirofilaria immitis polyprotein that stimulates murine B cells to produce nonspecific polyclonal immunoglobulin E antibody. Infect Immun 70:1235–1244

  90. Tezuka H, Imai S, Hidano S, Tsukidate S, Fujita K (2003) Various types of Dirofilaria immitis polyproteins selectively induce a Th2-type immune response. Infect Immun 71:3802–3811

  91. Tuomilehto J (2013) The emerging global epidemic of type 1 diabetes. Curr Diab Rep 13:795–804

  92. Walsh KP, Brady MT, Finlay CM, Boon L, Mills KH (2009) Infection with a helminth parasite attenuates autoimmunity through TGF-beta-mediated suppression of Th17 and Th1 responses. J Immunol 183:1577–1586

  93. Wang A, Fernando M, Leung G, Phan V, Smyth D, McKay DM (2010) Exacerbation of oxazolone colitis by infection with the helminth Hymenolepis diminuta: involvement of IL-5 and eosinophils. Am J Pathol 177:2850–2859

  94. Whelan RA, Hartmann S, Rausch S (2012) Nematode modulation of inflammatory bowel disease. Protoplasma 249:871–886

  95. Wilson MS et al (2010) Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur J Immunol 40:1682–1696

  96. Wirtz S, Neufert C, Weigmann B, Neurath MF (2007) Chemically induced mouse models of intestinal inflammation. Nat Protoc 2:541–546

  97. Wu Z, Nagano I, Asano K, Takahashi Y (2010) Infection of non-encapsulated species of Trichinella ameliorates experimental autoimmune encephalomyelitis involving suppression of Th17 and Th1 response. Parasitol Res 107:1173–1188

  98. Yamaoka KA, Kolb JP, Miyasaka N, Inuo G, Fujita K (1994) Purified excretory-secretory component of filarial parasite enhances Fc epsilon RII/CD23 expression on human splenic B and T cells and IgE synthesis while potentiating T-helper type 2-related cytokine generation from T cells. Immunology 81:507–512

  99. Yousefi F, Ebtekar M, Soleimani M, Soudi S, Hashemi SM (2013) Comparison of in vivo immunomodulatory effects of intravenous and intraperitoneal administration of adipose-tissue mesenchymal stem cells in experimental autoimmune encephalomyelitis (EAE). Int Immunopharmacol 17:608–616

  100. Zaccone P, Hall SW (2012) Helminth infection and type 1 diabetes. Rev Diabet Stud 9:272–286

  101. Zaccone P, Fehervari Z, Jones FM, Sidobre S, Kronenberg M, Dunne DW, Cooke A (2003) Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur J Immunol 33:1439–1449

  102. Zaccone P, Fehervari Z, Phillips JM, Dunne DW, Cooke A (2006) Parasitic worms and inflammatory diseases. Parasite Immunol 28:515–523

  103. Zaccone P, Burton O, Miller N, Jones FM, Dunne DW, Cooke A (2009) Schistosoma mansoni Egg antigens induce Treg that participate in diabetes prevention in NOD mice. Eur J Immunol 39:1098–1107

  104. Zaccone P, Burton OT, Gibbs S, Miller N, Jones FM, Dunne DW, Cooke A (2010) Immune modulation by Schistosoma mansoni antigens in NOD mice: effects on both innate and adaptive immune systems. J Biomed Biotechnol 2010:795210

  105. Zaccone P et al (2011) The S. mansoni glycoprotein omega-1 induces Foxp3 expression in NOD mouse CD4(+) T cells. Eur J Immunol 41:2709–2718

  106. Zhang R et al (2016) CD226 ligation protects against EAE by promoting IL-10 expression via regulation of CD4+ T cell differentiation. Oncotarget 7:19251–19264

  107. Zheng X, Hu X, Zhou G, Lu Z, Qiu W, Bao J, Dai Y (2008) Soluble egg antigen from Schistosoma japonicum modulates the progression of chronic progressive experimental autoimmune encephalomyelitis via Th2-shift response. J Neuroimmunol 194:107–114

  108. Zheng XP, Zhang HL, Li HF, Zhang MZ, Qiu W, Hu XQ (2012) Neuroprotective potential beyond immunoregulation of helminth infection as a therapeutic target in multiple sclerosis. Med Hypotheses 78:95–97

  109. Ziegler T et al (2015) A novel regulatory macrophage induced by a helminth molecule instructs IL-10 in CD4+ T cells and protects against mucosal inflammation. J Immunol 194:1555–1564

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Acknowledgements

This work was supported by grants from the National Key Research and Development Program of China (grant no. 2016YFC1202003, 2016YFC1202005 and 2016YFC1200500), Project of Basic Platform of National Science and Technology Resources of Ministry of Sciences and Technology of China (grant no. TDRC-2017-22), the National Natural Science Foundation of China (grant no. 81371836, 81572023 and 81271855), Guangdong Natural Science Foundation (grant no. 2014A030313134), Science and Technology Planning Project of Guangdong Province (grant no. 2016A050502008), Science and Technology Planning Project of Guangzhou (grant no. 201607010029), the 111 Project (grant no. B12003), the Undergraduates Innovation Training Program of Guangdong Province (grant no. 201410558274 and 201601084) and Teaching Reform Project of Sun Yat-sen University (grant no. 2016012).

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Correspondence to Zhiyue Lv.

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Wang Meng, Wu Linxiang, Weng Rennan, Zheng Weihong are the joint first authors.

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Wang, M., Wu, L., Weng, R. et al. Therapeutic potential of helminths in autoimmune diseases: helminth-derived immune-regulators and immune balance. Parasitol Res 116, 2065–2074 (2017). https://doi.org/10.1007/s00436-017-5544-5

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Keywords

  • Helminths
  • Autoimmune diseases
  • Therapeutic potential
  • Immune balance